Trans-species polymorphism and allele-specific expression in the cbf gene family of wild tomatoes

Molecular Biology and Evolution

Volumn 29, Issue 12, 2012, Pages 3641-3652

  Mboup, Mamadou ^a   Fischer, Iris ^a   Lainer, Hilde ^a   Stephan, Wolfgang ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

adaptation; allele specific expression; balancing selection; CBF (C repeat binding factor); trans species polymorphism; wild tomatoes

Indexed keywords

C REPEAT BINDING FACTOR; NUCLEIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG;

ABIOTIC STRESS; ALLELE; ALLELE SPECIFIC EXPRESSION; BALANCING SELECTION; CBF GENE; COLD STRESS; COLD TOLERANCE; CONFERENCE PAPER; DROUGHT STRESS; GENE; GENE CONVERSION; GENE EXPRESSION; GENE LOCUS; GENETIC RESOURCE; HABITAT; NONHUMAN; NUCLEOTIDE SEQUENCE; PSEUDOGENE; PURIFYING SELECTION; SOLANUM CHILENSE; SOLANUM PERUVIANUM; TOMATO;

ADAPTATION, BIOLOGICAL; CHILE; COLD TEMPERATURE; DROUGHTS; GENE CONVERSION; GENE EXPRESSION PROFILING; GENETIC VARIATION; GENETICS, POPULATION; LIKELIHOOD FUNCTIONS; LYCOPERSICON ESCULENTUM; MODELS, GENETIC; PERU; PLANT PROTEINS; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

LYCOPERSICON ESCULENTUM; LYCOPERSICON PERUVIANUM;

EID: 84869045708     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss176     Document Type: Conference Paper

References (77)

1. Arunyawat U, Stephan W, Stadler T. 2007. Using multilocus sequence data to assess population structure, natural selection, and linkage disequilibrium in wild tomatoes. Mol Biol Evol. 24:2310-2322.
2. Baker SS, Wilhelm KS, Thomashow MF. 1994. The 50-region of Arabidopsis-Thaliana Cor15a has cis-acting elements that confer cold-regulated, drought-regulated and aba-regulated geneexpression. Plant Mol Biol. 24:701-713.
3. Balakirev ES, Ayala FJ. 2003. Pseudogenes: are they junk or functional DNA? Annu Rev Genet. 37:123-151.
4. Bartels D, Sunkar R. 2005. Drought and salt tolerance in plants. Crit Rev Plant Sciences. 24:23-58.
5. Baudry E, Kerdelhue C, Innan H, Stephan W. 2001. Species and recombination effects on DNA variability in the tomato genus. Genetics 158:1725-1735.
6. Beaumont MA, Balding DJ. 2004. Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol. 13:969-980.
7. Bohnert HJ, Nelson DE, Jensen RG. 1995. Adaptations to environmental stresses. Plant Cell. 7:1099-1111.
8. Carpenter JF, Crowe JH. 1989. An infrared spectroscopic study of the interactions of carbohydrates with dried proteins. Biochemistry. 28: 3916-3922.
9. Castric V, Bechsgaard J, Schierup MH, Vekemans X. 2008. Repeated adaptive introgression at a gene under multiallelic balancing selection. Plos Genet. 4(8):e1000168.
10. Chetelat RT, Pertuze RA, Faundez L, Graham EB, Jones CM. 2009. Distribution, ecology and reproductive biology of wild tomatoes and related nightshades from the Atacama Desert region of northern Chile. Euphytica. 167:77-93.
11. Chinnusamy V, Zhu J, Zhu JK. 2007. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12:444-451.
12. Fischer I, Camus-Kulandaivelu L, Allal F, Stephan W. 2011. Adaptation to drought in two wild tomato species: the evolution of the Asr gene family. New Phytol. 190:1032-1044.
13. Force A, Lynch M, Postlethwait J. 1999. Preservation of duplicate genes by subfunctionalization. Am Zool. 39:460.
14. Fowler S, Thomashow MF. 2002. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell. 14:1675-1690.
15. Fu YX, Li WH. 1993. Statistical tests of neutrality of mutations. Genetics. 133:693-709.
16. Gilmour SJ, Fowler SG, Thomashow MF. 2004. Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol. 54:767-781.
17. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF. 2000. Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 124:1854-1865.
18. Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS. 2004. Allelic variation of gene expression in maize hybrids. Plant Cell. 16: 1707-1716.
19. Hey J,Wakeley J. 1997. A coalescent estimator of the population recombination rate. Genetics 145:833-845.
20. Hudson RR, Kreitman M, Aguade M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153-159.
21. Innan H. 2003. The coalescent and inEnite-site model of a small multigene. Genetics 163:803-810.
22. Innan H, Kondrashov F. 2010. The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet. 11: 97-108.
23. Jost L. 2008. GST and its relatives do not measure differentiation. Mol Ecol. 17:4015-4026.
24. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1999. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol. 17: 287-291.
25. Keane TM, Goodstadt L, Danecek P, et al.. 2011. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477: 289-294.
26. Klein J, Sato A, Nagl S, O'huigin C. 1998. Molecular trans-species polymorphism. Annu Rev Ecol Syst. 29:1-21.
27. Li WH, Gojobori T, Nei M. 1981. Pseudogenes as a paradigm of neutral evolution. Nature 292:237-239.
28. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
29. Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JDG, Romeis T. 2005. Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci U S A. 102: 10736-10741.
30. Lynch M, Force A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459-473.
31. Maskin L, Gudesblat GE, Moreno JE, Carrari FO, Frankel N, Sambade A, Rossi M, Iusem ND. 2001. Differential expression of the members of the Asr gene family in tomato (Lycopersicon esculentum). Plant Sci. 161:739-746.
32. Mcdonald JH, KreitmanM. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
33. Moore RC, Purugganan MD. 2005. The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol. 8:122-128.
34. Navarro M, Marque G, Ayax C, Keller G, Borges JP, Marque C, Teulieres C. 2009. Complementary regulation of four eucalyptus CBF genes under various cold conditions. J Exp Bot. 60:2713-2724.
35. Novillo F, Alonso JM, Ecker JR, Salinas J. 2004. CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in, stress tolerance in Arabidopsis. Proc Natl Acad Sci U S A. 101:3985-3990.
36. Novillo F, Medina J, Salinas J. 2007. Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci U S A. 104: 21002-21007.
37. Ohno S. 1970. Evolution by gene duplication. New York: Springer-Verlag.
38. Ohno R, Takumi S, Nakamura C. 2001. Expression of a cold-responsive Lt-Cor gene and development of freezing tolerance during cold acclimation in wheat (Triticum aestivum L.). J Exp Bot. 52: 2367-2374.
39. O'huigin C. 1995. Quantifying the degree of convergence in primate mhc-drb genes. Immunol Rev. 143:123-140.
40. O'Neill SD. 1983. Osmotic adjustment and the development of freezing resistance in Fragaria virginiana. Plant Physiol. 72:938-944.
41. Palacios R, Gazave E, Goni J, Piedrafita G, Fernando O, Navarro A, Villoslada P. 2009. Allele-specific gene expression is widespread across the genome and biological processes. Plos One. 4(1):e4150.
42. Pennycooke JC, Cheng HM, Roberts SM, Yang QF, Rhee SY, Stockinger EJ. 2008. The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements. Plant Mol Biol. 67:483-497.
43. Peralta IE, Spooner DM, Knapp S. 2008. Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Juglandifolia, sect. Lycopersicon; Solanaceae). Syst Bot Monogr. 84:1-186.
44. Perras M, Sarhan F. 1984. Energy-state of spring and winter-wheat during cold hardening-soluble sugars and adenine-nucleotides. Physiol Plantarum. 60:129-132.
45. Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamagushi-Shinozaki KY. 2004. Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol. 45:1042-1052.
46. Riebler A, Held L, Stephan W. 2008. Bayesian variable selection for detecting adaptive genomic differences among populations. Genetics 178:1817-1829.
47. Roselius K, Stephan W, Stadler T. 2005. The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 171:753-763.
48. Sakai A, Yoshida S. 1968. The role of sugar and related compounds in variations of freezing resistance. Cryobiology 5:160-174.
49. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K. 2001. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell. 13:61-72.
50. Sota T, Ishikawa R, Ujiie M, Kusumoto F, Vogler AP. 2001. Extensive trans-species mitochondrial polymorphisms in the carabid beetles Carabus subgenus Ohomopterus caused by repeated introgressive hybridization. Mol Ecol. 10:2833-2847.
51. Stadler T, Arunyawat U, Stephan W. 2008. Population genetics of speciation in two closely related wild tomatoes (Solanum section lycopersicon). Genetics 178:339-350.
52. Stadler T, Haubold B, Merino C, Stephan W, Pfaffelhuber P. 2009. The impact of sampling schemes on the site frequency spectrum in nonequilibrium subdivided populations. Genetics 182:205-216.
53. Stadler T, Roselius K, Stephan W. 2005. Genealogical footprints of speciation processes in wild tomatoes: demography and evidence for historical gene flow. Evolution 59:1268-1279.
54. Stockinger EJ, Gilmour SJ, Thomashow MF. 1997. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci U S A. 94:1035-1040.
55. Tajima F. 1983. Evolutionary relationship of DNA-sequences in finite populations. Genetics 105:437-460.
56. Tajima F. 1989. Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
57. Tellier A, Fischer I, Merino C, Xia H, Camus-Kulandaivelu L, Stadler T, Stephan W. 2011. Fitness effects of derived deleterious mutations in four closely related wild tomato species with spatial structure. Heredity 107:189-199.
58. Tellier A, Laurent SJ, Lainer H, Pavlidis P, Stephan W. 2011. Inference of seed bank parameters in two wild tomato species using ecological and genetic data. Proc Natl Acad Sci U S A. 108:17052-17057.
59. Thomashow MF. 2010. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol. 154:571-577.
60. Travert S, Valerio L, Fouraste I, Boudet AM, Teulieres C. 1997. Enrichment in specific soluble sugars of two Eucalyptus cell-suspension cultures by various treatments enhances their frost tolerance via a noncolligative mechanism. Plant Physiol. 114:1433-1442.
61. Vagujfalvi A, Galiba G, Cattivelli L, Dubcovsky J. 2003. The cold-regulated transcriptional activator CBF3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol Genet Genomics. 269:60-67.
62. Venema JH, Linger P, van Heusden AW, van Hasselt PR, BruggemannW. 2005. The inheritance of chilling tolerance in tomato (Lycopersicon spp.). Plant Biol. 7:118-130.
63. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF. 2005. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 41: 195-211.
64. von Korff M, Radovic S, Choumane W, et al. 2009. Asymmetric allele-specific expression in relation to developmental variation and drought stress in barley hybrids. Plant J. 59:14-26.
65. Watterson GA. 1975. Number of segregating sites in genetic models without recombination. Theor Popul Biol. 7:256-276.
66. Wright SI, Charlesworth B. 2004. The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 168: 1071-1076.
67. Xia H, Camus-Kulandaivelu L, Stephan W, Tellier A, Zhang ZW. 2010. Nucleotide diversity patterns of local adaptation at drought-related candidate genes in wild tomatoes. Mol Ecol. 19:4144-4154.
68. Yamada K, Lim J, Dale JM, et al.. 2003. Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302: 842-846.
69. Yamaguchi-Shinozaki K, Shinozaki K. 1994. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought low temperature, or high-salt stress. Plant Cell. 6:251-264.
70. Yamaguchi-Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol. 57:781-803.
71. Yanez M, Caceres S, Orellana S, Bastias A, Verdugo I, Ruiz-Lara S, Casaretto J. 2009. An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Rep. 28:1497-1507.
72. Young KR, Ulloa CU, Luteyn JL, Knapp S. 2002. Plant evolution and endemism in Andean South America: an introduction. Bot Rev. 68:4-21.
73. Zhang X, Borevitz JO. 2009. Global analysis of allele-specific expression in Arabidopsis thaliana. Genetics 182:943-954.
74. Zhang X, Fowler SG, Cheng H, Lou Y, Rhee SY, Stockinger EJ, Thomashow MF. 2004. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J. 39: 905-919.
75. Zhen Y, Ungerer MC. 2008. Relaxed selection on the CBF/DREB1 regulatory genes and reduced freezing tolerance in the southern range of Arabidopsis thaliana. Mol Biol Evol. 25:2547-2555.
76. Zheng DY, Gerstein MB. 2007. The ambiguous boundary between genes and pseudogenes: the dead rise up, or do they? Trends Genet. 23: 219-224.
77. Zou C, Lehti-Shiu MD, Thibaud-Nissen F, Prakash T, Buell CR, Shiu SH. 2009. Evolutionary and expression signatures of pseudogenes in Arabidopsis and rice. Plant Physiol. 151:3-15.